Summary
In this study, electron microscopy was used to study cell clustering in the postnatal mouse striatum. From the date of birth (PO) through postnatal day 7 (P7), groupings of eight to ten striatal neurons were delimited easily in low magnification electron micrographs. Often, within individual groupings, adjacent neurons were separated only by a thin, 10 nm gap, and formed cell pairs or cell triads. Coincident with marked expansion of the striatal neuropil in the second postnatal week, striatal neurons formed more dispersed cell clusters consisting only occasionally of cell pairs or triads.
Single, pyknotic neuronal nuclei were seen in clusters of normal neurons exhibiting different stages of maturation but were absent from clusters consisting only of well-differentiated neurons. The neuropil surrounding cell clusters with pyknotic neurons or that adjacent to neighboring cell clusters often contained degenerating dendrites and axon terminals. Whereas this naturally occurring neuronal cell death was present in the tissue throughout the first postnatal week, only degenerating dendritic and axonal profiles were seen in the P15 striatum. This latter fact suggests that the occurrence of pyknotic neuronal somata does not account entirely for the more localized degeneration of other neuronal profiles and raises the possibility that other degenerative processes may be occurring simultaneously in the tissue.
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References
Adinolfi AM (1977) The postnatal development of the caudate nucleus: A Golgi and electron microscopic study of kittens. Brain Res 133:251–266
Aguayo AJ, Peyronnard JM, Terry LC, Romine LS, Bray GM (1976) Neonatal neuronal loss in rat superior cervical ganglia: Retrograde effects on developing preganglionic axons and Schwann cells. J Neurocytol 5:137–155
Angevine Jr JB, McConnell JA (1974) Time of origin of striatal neurons in the mouse: An autoradiographic study. Anat Rec 178:300
Arees EA, Aström KE (1977) Cell death in the optic tectum of the developing rat. Anat Embryol 151:29–34
Bodian D (1966) Spontaneous degeneration in the spinal cord of the monkey fetuses. Johns Hopkins Hosp Bull 119:212–234
Brand S, Rakic P (1978) Time of origin of neurons in primate neostriatum: H3-thymidine autoradiographic analysis in the rhesus monkey. Anat Rec 190:345
Butcher LL, Hodge GK (1976) Postnatal development of acetylcholinesterase in the caudate-putamen nucleus and substantia nigra of rats. Brain Res 106:223–240
Cantino D, Daneo LS (1972) Cell death in the developing chick optic tectum. Brain Res 38:13–25
Changeux J-P, Danchin A (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264:705–712
Chu-Wang I-Wu, Oppenheim RW (1978a) Cell death of motoneurons in the chick embryo spinal cord. I. A light and electron microscopic study of naturally occurring and induced cell loss during development. J Comp Neurol 177:33–58
Chu-Wang I-Wu, Oppenheim RW (1978b) Cell death of motoneurons in the chick embryo spinal cord. II. A quantitative and qualitative analysis of degeneration in the ventral root, including evidence for axon outgrowth and limb innervation prior to cell death. J Comp Neurol 177:59–86
Clarke PGH, Cowan WM (1975) Ectopic neurons and aberrant connections during neural development. Proc Natl Acad Sci USA 72:4455–4458
Cospito JA, Levine MS, Adinolfi AM (1980) Organization of developing precruciate corticostriate projections in kittens. Exp Neurol 67:447–452
Cowan WM (1973) Neuronal death as a regulative mechanism in the control of cell number in the nervous system. In: Rockstein M (ed) Development and aging in the nervous system. Academic Press, New York, pp 19–41
DiFiglia M, Pasik P, Pasik T (1980a) Early postnatal developmental of the monkey neostriatum: A Golgi and ultrastructural study. J Comp Neurol 190:303–331
DiFiglia M, Pasik T, Pasik P (1980b) Ultrastructure of Golgi-impregnated and gold-toned spiny and aspiny neurons in the monkey neostriatum. J Neurocytol 9:471–492
Flanagan AEH (1969) Differentiation and degeneration in the motor horn of the foetal mouse. J Morphol 129:281–306
Glucksmann A (1951) Cell deaths in normal vertebrate ontogeny. Biol Rev 26:59–86
Goldman PS, Nauta WJH (1977) An intricately patterned prefronto-caudate projection in the rhesus monkey. J Comp Neurol 171:369–386
Graybiel AM, Ragsdale Jr CW (1980) Clumping of acetylcholinesterase activity in the developing striatum of the human fetus and young infant. Proc Natl Acad Sci USA 77:1214–1218
Hamburger V (1975) Cell death in the development of the lateral motor column of the chick embryo. J Comp Neurol 160:535–546
Hamburger V, Brunso-Bechthold JK, Yip JW (1981) Neuronal death in the spinal ganglia of the chick embryo and its reduction by nerve growth factor. J Neurosci 1:60–71
Hattori T, McGeer PL (1973) Synaptogenesis in the corpus striatum of infant rat. Exp Neurol 38:70–79
Heumann D, Reuber G, Rabinowicz T (1978) Postnatal development of the mouse cerebral cortex. IV. Evolution of the total cortical volume of the population of neurons and glial cells. J Hirnforsch 19:385–393
Hollyday M, Hamburger V (1976) Reduction of the naturally occurring motor neuron loss by enlargement of the periphery. J Comp Neurol 170:311–320
Johnson TN, Rosvold HE, Galkin TW, Goldman PS (1976) Postnatal maturation of subcortical projections from the prefrontal cortex in the rhesus monkey. J Comp Neurol 166:427–444
Laing NG, Prestige MC (1978) Prevention of spontaneous motoneurone death in chick embryos. J Physiol (Lond) 282:33–34P
Mensah PL (1977) The internal organization of the mouse caudate nucleus. Evidence for cell clustering and regional variation. Brain Res 137:53–66
Mensah PL (1980) Distribution of the largest neuron in mouse caudate-putamen nucleus: Its position in large cell-medium cell clusters. Exp Brain Res 38:267–271
Mensah PL (1982) Stability of large cell-medium cell clusters in the mature neostriatum. Exp Brain Res, in press
Nobin A, Björklund A (1973) Topography of the monamine neuron systems in the human brain as revealed in fetuses. Acta Physiol Scand 88 (Suppl 388):1–40
Olson L, Seiger A, Fuxe K (1972) Heterogeneity of striatal and limbic dopamine innervation: Highly fluorescent islands in developing and adult rats. Brain Res 44:283–288
Oppenheim RW (1975) Progress and challenges in neuroembryology. Bioscience 25:28–36
Oppenheim RW (1981) Neuronal cell death and some related regressive phenomena during neurogenesis: A selective historical review and progress report. In: Cowan WM (ed) Studies in developmental neurobiology: Essays in honor of Viktor Hamburger, Oxford University Press, pp 74–133
Oppenheim RW, Chu-Wang I-Wu (1977) Spontaneous cell death of spinal motoneurons following peripheral innervation in the chick embryo. Brain Res 125:154–160
Pannese E (1976) An electron microscopic study of cell degeneration in chick embryo spinal ganglia. Neuropath App Neurobiol 2:247–267
Pannese E, Luciano L, Iurato S, Reale E (1976) Lysosomes in normal and degenerating neuroblasts of the chick embryo spinal ganglia. Ann Neuropath 36:209–220
Pittman RH, Oppenheim RW (1978) Neuromuscular blockade increases motoneuron survival during normal cell death in the chick embryo. Nature 271:364–366
Prestige MC (1976) Evidence that at least some of the motor nerve cells that die during development have first made peripheral connections. J Comp Neurol 170:123–134
Purves D, Lichtman JW (1980) Elimination of synapses in the developing nervous system. Science 210:153–157
Richardson KC, Jarret L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323
Sohal GS (1976) An experimental study of cell death in the developing trochlear nucleus. Exp Neurol 51:684–698
Sohal GS (1977) Development of the oculomotor nucleus, with special reference to the time of cell origin and cell death. Brain Res 138:217–228
Sohal GS, Holt RK (1977) Cell death during normal development of the abducens nucleus. Exp Neurol 54:533–545
Sohal GS, Weidman TA (1978) Ultrastructural sequence of embryonic cell death in normal and peripheral deprived trochlear nucleus. Exp Neurol 61:53–64
Somogyi P, Bolam JP, Smith AD (1981) Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure. J Comp Neurol 195:567–584
Sotelo C, Changeux J-P (1974) Transsynaptic degeneration “en cascade” in the cerebellar cortex of staggerer mutant mice. Brain Res 67:519–526
Sotelo C, Palay SL (1971) Altered axons and axon terminals in the lateral vestibular nucleus of the rat: Possible example of axonal remodeling. Lab Invest 25:653–671
Sturrock RR (1979) A quantitative lifespan study of changes in cell number, cell division and cell death in various regions of the mouse forebrain. Neuropath App Neurobiol 5:433–456
Sturrock RR (1980) A developmental study of the mouse neostriatum. J Anat 130:243–261
Tanaka Jr D, Alexander B (1978) Golgi and electron microscopic evidence for growth cones in the caudate nucleus of the neonatal dog. Exp Neurol 60:614–623
Tennyson VM, Barrett RE, Cohen G, Cote L, Heikkila R, Mytilineou C (1972) The developing neostriatum of the rabbit: Correlation of fluorescence histochemistry, electron microscopy, endogenous dopamine levels, and 3H dopamine uptake. Brain Res 46:251–285
Weiss GM, Pysh JJ (1978) Evidence for loss of Purkinje cell dendrites during late development: A morphometric Golgi analysis in the mouse. Brain Res 154:219–230
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Mensah, P.L. An electron microscopical study of neuronal cell clustering in postnatal mouse striatum, with special emphasis on neuronal cell death. Anat Embryol 164, 387–401 (1982). https://doi.org/10.1007/BF00315760
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DOI: https://doi.org/10.1007/BF00315760